Mating system variation drives rapid evolution of the female transcriptome in Drosophila pseudoobscura

Ecology and Evolution

Volumn 4, Issue 11, 2014, Pages 2186-2201

  Immonen, Elina ^a,b   Snook, Rhonda R ^c   Ritchie, Michael G ^a  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Drosophila; Gene expression; Microarray; Polyandry; Sexual selection

Indexed keywords

EID: 84901785377     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.1098     Document Type: Article

References (63)

1. Anderson, W. W. 1974. Frequent multiple insemination in a natural population of Drosophila pseudoobscura. Am. Nat. 108:709-711.
2. Andersson, M., and L. W. Simmons. 2006. Sexual selection and mate choice. Trends Ecol. Evol. 21:296-302.
3. Arnqvist, G., and T. Nilsson. 2000. The evolution of polyandry: multiple mating and female fitness in insects. Anim. Behav. 60:145-164.
4. Avila, F. W., L. K. Sirot, B. A. LaFlamme, C. D. Rubinstein, and M. F. Wolfner. 2011. Insect seminal fluid proteins: identification and function. Ann. Rev. Entom. 56:21-40.
5. Bacigalupe, L. D., H. S. Crudgington, J. Slate, A. J. Moore, and R. R. Snook. 2008. Sexual selection and interacting phenotypes in experimental evolution: a study of Drosophila pseudoobscura mating behavior. Evolution 62:1804-1812.
6. Benjamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. B 57:289-300.
7. Birkhead, T. R., and T. Pizzari. 2002. Postcopulatory sexual selection. Nature Rev. Genet. 3:262-273.
8. Brown, W. D., A. Bjork, K. Schneider, and S. Pitnick. 2004. No evidence that polyandry benefits females in Drosophila melanogaster. Evolution 58:1242-1250.
9. Chapman, T., L. F. Liddle, J. M. Kalb, M. F. Wolfner, and L. Partridge. 1995. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373:241-244.
10. Chapman, T., G. Arnqvist, J. Bangham, and L. Rowe. 2003. Sexual conflict. Trends Ecol. Evol. 18:41-47.
11. Chintapalli, V. R., J. Wang, and J. A. Dow. 2007. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat. Genet. 39:715-720.
12. Crudgington, H. S., and M. T. Siva-Jothy. 2000. Genital damage, kicking and early death - The battle of the sexes takes a sinister turn in the bean weevil. Nature 407:855-856.
13. Crudgington, H. S., A. P. Beckerman, L. Brustle, K. Green, and R. R. Snook. 2005. Experimental removal and elevation of sexual selection: does sexual selection generate manipulative males and resistant females? Am. Nat. 165:S72-S87.
14. Crudgington, H. S., S. Fellows, N. S. Badcock, and R. R. Snook. 2009. Experimental manipulation of sexual selection promotes greater male mating capacity but does not alter sperm investment. Evolution 63:926-938.
15. Crudgington, H. S., S. Fellows, and R. R. Snook. 2010. Increased opportunity for sexual conflict promotes harmful males with elevated courtship frequencies. J. Evol. Biol. 23:440-446.
16. Cummings, M. E., J. Larkins-Ford, C. R. L. Reilly, R. Y. Wong, M. Ramsey, and H. A. Hofmann. 2008. Sexual and social stimuli elicit rapid and contrasting genomic responses. Proc. Roy. Soc. B 275:393-402.
17. Dalton, J. E., T. S. Kacheria, S. R. Knott, M. S. Lebo, A. Nishitani, L. E. Sanders, et al. 2010. Dynamic, mating-induced gene expression changes in female head and brain tissues of Drosophila melanogaster. Bmc Genomics 11:541.
18. Dennis, G. J., B. T. Sherman, D. A. Hosack, J. Yang, W. Gao, H. C. Lane, et al. 2003. DAVID: database for Annotation, Visualization, and Integrated Discovery. Gen. Biol. 4:P3.
19. Ellegren, H., and J. Parsch. 2007. The evolution of sex-biased genes and sex-biased gene expression. Nature Rev. Genet. 8:689-698.
20. Franklin, A. M., Z. E. Squires, and D. Stuart-Fox. 2012. The energetic cost of mating in a promiscuous cephalopod. Biol. Lett. 8:754-756.
21. Gentleman, R. C., V. J. Carey, D. M. Bates, B. Bolstad, M. Dettling, S. Dudoit, et al. 2004. Bioconductor: open software development for computational biology and bioinformatics. Gen. Biol. 5:R80.
22. Gentleman, R., V. Carey, W. Huber, and F. Hahne. 2011. Genefilter: methods for filtering genes from microarray experiments, v 1.34.0.
23. Gnad, F., and J. Parsch. 2006. Sebida: a database for the functional and evolutionary analysis of genes with sex-biased expression. Bioinformatics 22:2577-2579.
24. Gowaty, P. A., Y. K. Kim, J. Rawlings, and W. W. Anderson. 2010. Polyandry increases offspring viability and mother productivity but does not decrease mother survival in Drosophila pseudoobscura. PNAS 107:13771-13776.
25. Holland, B., and W. R. Rice. 1998. Chase-away sexual selection: antagonistic seduction versus resistance. Evolution 52:1-7.
26. Holland, B., and W. R. Rice. 1999. Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. PNAS 96:5083-5088.
27. Hollis, B., D. Houle, Z. Yan, T. J. Kawecki, and L. Keller. 2014. Evolution under monogamy feminizes gene expression in Drosophila melanogaster. Nature Comm. 5:3482.
28. Huang, D. W., B. T. Sherman, and R. A. Lempicki. 2009. Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat. Protoc. 4:44-57.
29. Hughes, W. O. H., B. P. Oldroyd, M. Beekman, and F. L. W. Ratnieks. 2008. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213-1216.
30. Immonen, E., and M. G. Ritchie. 2012. The genomic response to courtship song stimulation in female Drosophila melanogaster. Proc. Roy. Soc. B 279:1359-1365.
31. Innocenti, P., and E. H. Morrow. 2009. Immunogenic males: a genome-wide analysis of reproduction and the cost of mating in Drosophila melanogaster females. J. Evol. Biol. 22:964-973.
32. Innocenti, P., E. H. Morrow, and D. K. Dowling. 2011. Experimental evidence supports a sex-specific selective sieve in mitochondrial genome evolution. Science 332:845-848.
33. Jennions, M. D., and M. Petrie. 2000. Why do females mate multiply? A review of the genetic benefits. Biol. Rev. Camb. Phil. Soc 75:21-64.
34. Jiang, Z. F., and C. A. Machado. 2009. Evolution of sex-dependent gene expression in three recently diverged species of Drosophila. Genetics 183:1175-1185.
35. Kokko, H., M. D. Jennions, and R. Brooks. 2006. Unifying and testing models of sexual selection. Annu. Rev. Ecol. Evol. Syst. 37:43-66.
36. Kvarnemo, C., and L. W. Simmons. 2013. Polyandry as a mediator of sexual selection before and after mating. Phil. Trans. Roy. Soc. Lond. B 368:20120042.
37. Lehtonen, J., M. D. Jennions, and H. Kokko. 2012. The many costs of sex. Trends Ecol. Evol. 27:172-178.
38. Mack, P. D., A. Kapelnikov, Y. Heifetz, and M. Bender. 2006. Mating-responsive genes in reproductive tissues of female Drosophila melanogaster. PNAS 103:10358-10363.
39. Mank, J. E., L. Hultin-Rosenberg, E. Axelsson, and H. Ellegren. 2007. Rapid evolution of female-biased, but not male-biased, genes expressed in the avian brain. Mol. Biol. Evol. 24:2698-2706.
40. Mank, J. E., N. Wedell, and D. J. Hosken. 2013. Polyandry and sex-specific gene expression. Phil. Trans. Roy. Soc. Lond. B 368:20120047.
41. Martin, O. Y., and D. J. Hosken. 2003. The evolution of reproductive isolation through sexual conflict. Nature 423:979-982.
42. McGraw, L. A., G. Gibson, A. G. Clark, and M. F. Wolfner. 2004. Genes regulated by mating, sperm, or seminal proteins in mated female Drosophila melanogaster. Curr. Biol. 14:1509-1514.
43. McGraw, L. A., A. G. Clark, and M. F. Wolfner. 2008. Post-mating gene expression profiles of female Drosophila melanogaster in response to time and to four male accessory gland proteins. Genetics 179:1395-1408.
44. Meisel, R. P., J. H. Malone, and A. G. Clark. 2012. Disentangling the relationship between sex-biased gene expression and X-linkage. Gen. Res. 22:1255-1265.
45. Parker, G. A. 1979. Sexual selection and sexual conflict. Pp. 123-166 in M. S. Blum, N. A. Blum, eds. Sexual selection and reproductive competition in insects. Academic Press, London.
46. Parker, G. A. 2006. Sexual conflict over mating and fertilization: an overview. Phil. Trans. Roy. Soc. Lond. B 361:235-259.
47. Pointer, M. A., P. W. Harrison, A. E. Wright, and J. E. Mank. 2013. Masculinization of gene expression is associated with exaggeration of male sexual dimorphism. PLoS Genet. 9:e1003697.
48. Preuss, K. M., J. A. Lopez, J. K. Colbourne, and M. J. Wade. 2012. Identification of maternally-loaded RNA transcripts in unfertilized eggs of Tribolium castaneum. Bmc Genomics 13:671.
49. R Development Core Team. 2011. R: a language and environment for statistical computing. R Development Core Team, Vienna, Austria.
50. Rice, W. R. 1984. Sex chromosomes and the evolution of sexual dimorphism. Evolution 38:735-742.
51. Ritchie, M. G. 2007. Sexual selection and speciation. Ann. Rev. Ecol. Evol. Syst. 38:79-102.
52. Rung, J., and A. Brazma. 2013. Reuse of public genome-wide gene expression data. Nat. Rev. Genet. 14:89-99.
53. Slatyer, R. A., B. S. Mautz, P. R. Backwell, and M. D. Jennions. 2011. Estimating genetic benefits of polyandry from experimental studies: a meta-analysis. Biol. Rev. Camb. Phil. Soc. 87:1-33.
54. Smyth, G. K. 2004. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3:Article3.
55. Smyth, G. K. 2005. Limma: linear models for microarray data. Pp. 397-420 in R. Gentleman, V. Carey, S. Dudoit, R. Irizarry and W. Huber, eds. Bioinformatics and computational biology solutions using R and Bioconductor. Springer, New York.
56. Smyth, G. K., and T. P. Speed. 2003. Normalization of cDNA microarray data. Methods 31:265-273.
57. Snook, R. R., A. Robertson, H. S. Crudgington, and M. G. Ritchie. 2005. Experimental manipulation of sexual selection and the evolution of courtship song in Drosophila pseudoobscura. Behav. Genet. 35:245-255.
58. Snook, R. R., L. Brüstle, and J. Slate. 2009. A test and review of the role of effective population size on experimental sexual selection patterns. Evolution 63:1923-1933.
59. Snook, R. R., L. D. Bacigalupe, and A. J. Moore. 2010. The quantitative genetics and coevolution of male and female reproductive traits. Evolution 64:1926-1934.
60. Wigby, S., and T. Chapman. 2005. Sex peptide causes mating costs in female Drosophila melanogaster. Curr. Biol. 15:316-321.
61. Wigby, S., L. K. Sirot, J. R. Linklater, N. Buehner, F. C. Calboli, A. Bretman, et al. 2009. Seminal fluid protein allocation and male reproductive success. Curr. Biol. 19:751-757.
62. Wolf, J. B., E. D. Brodie Iii, J. M. Cheverud, A. J. Moore, and M. J. Wade. 1998. Evolutionary consequences of indirect genetic effects. Trends Ecol. Evol. 13:64-69.
63. Zhang, Y., D. Sturgill, M. Parisi, S. Kumar, and B. Oliver. 2007. Constraint and turnover in sex-biased gene expression in the genus Drosophila. Nature 450:233-237.